S. O. Voityuk, V. P. Heluta & E. Nevo

Neoerysiphe cumminsiana (Erysiphales, Eumycota), a new powdery mildew fungus in Israel

Abstract Voityuk, S. O., Heluta, V. P. & Nevo, E.: Neoerysiphe cumminsiana (Erysiphales, Eumycota), a new powdery mildew fungus in Israel. — Fl. Medit. 14: 267-273. 2004. — ISSN 1120-4052. Information is provided about the distribution of a powdery mildew fungus species new for Israel, Neoerysiphe cumminsiana (U. Braun) U. Braun (Erysiphales), recorded on spp. and Phagnalon rupestre (L.) DC. A conclusion is reached about the possibility of discovering this fungus in some countries of southern and in northern and southern . The need is noted for the revision of powdery mildew specimens identified as Erysiphe cichoracearum DC. and collected in these regions on host belonging to .

Introduction

Neoerysiphe cumminsiana (U. Braun) U. Braun is one of five species of the small Neoerysiphe U. Braun (Erysiphales, Eumycota). This species was described by Braun (1983) as Erysiphe cumminsiana U. Braun, based on the specimen of this fungus collect- ed on Senecio seemanii Sch.-Bip. (Asteraceae) in North America. After the section Golovinomyces U. Braun (genus Erysiphe R. Hedw. ex DC.) was raised to the genus level (Heluta 1988a), the species was transferred to this genus and named G. cumminsianus (U. Braun) Heluta (Heluta 1988b). However, some time later, on the basis of specific mor- phological characters, especially particulars of conidium surface features, formation of ascospores after wintering, morphology of appressoria, and results of molecular investiga- tions, some species from the genus Golovinomyces (U. Braun) Heluta, including G. cum- minsianus, were transferred to a new genus, Neoerysiphe (Braun 1999). Thus, the current- ly accepted name of the former Erysiphe cumminsiana is Neoerysiphe cumminsiana (U. Braun) U. Braun. N. cumminsiana is morphologically very similar to N. galeopsidis (DC.) U. Braun and N. galii (S. Blumer) U. Braun. All three species have ascocarps equally depressed in the lower part and completely maturing only after wintering, i.e., in a new vegetation period. Neoerysiphe cumminsiana differs from N. galeopsidis by the color of the appendages (they are hyaline, to yellowish, but not brownish), from N. galii, by the mainly lobed, not nip- ple-shaped appressoria although they can be of the two types in both species. In addition, 268 Voityuk & al.: Neoerysiphe cumminsiana (Erysiphales, Eumycota)...

N. cumminsiana is a parasite of Compositae (Asteraceae), N. galeopsidis parasitizing Labiatae (Lamiaceae), and N. galii was registered on host plants from Rubiaceae. Thus, since these three species are very similar, N. cumminsiana may be reported by mycologists as Erysiphe cumminsiana, E. galeopsidis, or E. galii. Amano (1986) reported E. cumminsiana or E. galeopsidis on Asteraceae as Bidens pilosa L. (Cuba), Cacalia del- phiniifolia Sieb. et Zucc. and C. tebakoensis Makino (Japan), L. (Germany), Eupatorium guadelupense Spreng. (South America), E. microstemon Cass. (Puerto Rico, USA), E. rugosum Houtt. (Canada and USA), Heliopsis helianthoides (L.) Sweet and H. helianthoides var. scabra (Dunal) Fisch. (USA), Ligularia fischeri (Ledeb.) Turcz. and L. stenocephala (Maxim.) Matsum. et Koidz. (Japan), Senecio seemanii Sch.-Bip. (USA), Tagetes sp. (Italy), and sp. (USA). Gorter (1987) reported E. galeopsidis on Arctotheca calendula (L.) Levyns from southern Africa; scanning electron micrographs testify that this fungus belongs to the genus Neoerysiphe. Havrylenko and Braun (1998) described Oidium baccharidis on Baccharis racemosa (Ruiz et Pavon) DC. from Argentina. It is probably an anamorph state of N. cumminsiana. According to Braun (1987), N. cumminsiana (sub E. cumminsiana) is recorded only on species of Cacalia, Eupatorium, Heliopsis, Ligularia, and Senecio in Asia (Japan) and North America (USA). In other monographs by this author on powdery mildew fungi of Europe (Braun 1995), finds of E. galeopsidis on Crepis biennis and Tagetes sp. are not mentioned and E. cumminsiana is not reported. Some time later, Heluta (1999) reported N. cumminsiana (sub G. cumminsianus) on Crepis micrantha Czer., C. rhoeadifolia M. Bieb., and Taraxacum sp. from the southern part of the Ukraine, mainly Crimea. In addi- tion, Heluta collected this fungus in Crimea in mid-April 2002 on a new host edulis P. Gaertn. (R. stellatus auct. non (L.) P. Gaertn.) (unpublished data). Thus, until the start of this investigation N. cumminsiana was known in fact from America, eastern Asia (Japan), southern Africa, and south eastern Europe (Ukraine, 10 localities) on representatives of the genera Arctotheca, Bidens, Cacalia, Crepis, Eupatorium, Heliopsis, Ligularia, Rhagadiolus, Senecio, and Taraxacum. Note, however, that this species was probably found also in other regions of Eurasia, but was misidenti- fied as another parasite of Asteraceae, Erysiphe cichoracearum DC., because Erysiphe (Neoerysiphe) cumminsiana has been described only recently.

Materials and methods

During our studies on phytopathogenic fungi of Israel, some specimens of powdery mildew fungi parasitizing Crepis spp. and Phagnalon rupestre (L.) DC. (Asteraceae) were collected. We identified all these fungi as Neoerysiphe cumminsiana. The specimens are listed below. On Crepis spp.: Mt. Carmel, Haifa, weed plant community, 15.03.2002, leg. V.P. Heluta; Carmel Coast, near Haifa, Atlit, coast of the , 19.03.2002, leg. V.P. Heluta (anamorph only); Sharon Plain, Pardes Hanna, 12.04.2002, leg. E. Nevo. On Phagnalon rupestre (L.) DC.: Upper Galilee, Nahal Keziv, “Evolution Canyon” II, “African”, south-facing slope, 18.03.2002, leg. T.V. Andrianova. Flora Mediterranea 14 — 2004 269

Fig. 1. Neoerysiphe cumminsiana (U. Braun) U. Braun: a-b - ascocarps from Crepis sp.; c - ascocarp from Phagnalon rupestre; d - asci; a - view from above, b - bottom view, c - side view; a-c - from Israel, d - from Ukraine.

Results

Microscope examinations showed that all these specimens had mycelium mainly with lobed appressoria, hemispheric ascocarps depressed in the lower part (Fig. 1, a-c) with hyaline or yellowish appendages. In all cases asci were immature. Specimens collected on Crepis spp. were practically identical with the Ukrainian specimens of N. cumminsiana, but the fungus from Phagnalon rupestre had somewhat larger ascocarps (123-190 µm in diameter) with faintly developed appendages. Probably, the last difference was caused through specific characters of the host plant. On the lower side of its leaves, a very dense layer of fibers had formed, which is of great importance in the fastening of ascocarps of N. cumminsiana, hence, in this case, appendages of the fungus remain underdeveloped. The integrated description of this fungus, including the morphological data about its Ukrainian specimens, is given below. 270 Voityuk & al.: Neoerysiphe cumminsiana (Erysiphales, Eumycota)...

Fig. 2. Distribution of N. cumminsiana in Israel: 1 - on Crepis sp.; 2 - on Phagnalon rupestre; 3 - pro- bably N. cumminsiana on Crepis spp. (literature data, sub Erysiphe cichoracearum). Natural regions of Israel: AP - Akko Plain; AV - Arava Valley; BS - Beit Shean Valley; CC - Carmel Coast; CM - Carmel Mts.; CN - Central Negev; DS - Dead Sea Area; EP - Esdraelon (Yizre'el) Plain; GH - Golan Heights; GM - Gilboa Mts.; HE - Hermon; HP - Hula Plain; JD - Judean Desert; JM - Judean Mts.; LG - Lower Galilee; LJ - Lower Jordan Valley; NN - Northern Negev; PP - Philistean Plain; SA - Samaria; SH - Shefela; SN - Southern Negev; SP - Sharon Plain; UG - Upper Galilee; UJ - Upper Jordan Valley; WN - Western Negev (after Feinbrun-Dothan, Danin, 1998) Flora Mediterranea 14 — 2004 271

Neoerysiphe cumminsiana (U. Braun) U. Braun, Schlechtendalia 3: 50 (1999) (Fig. 1) Syn.: Erysiphe galeopsidis auct., p.p.; E. cumminsiana U. Braun, Mycotaxon 18(1): 124 (1983); Golovinomyces cumminsianus (U. Braun) Heluta, Ukr. Bot. Zhurn. 45(5): 62 (1988)

Mycelium on all green parts of host plants, well developed, grey or yellowish by intense conidial sporulation, appressoria mainly lobed. Anamorph is Oidium s. str., conidia cylin- drical-ellipsoidal to vase-like, 22.5–38 x (10)13–19.5 µm. Cleistothecia scattered or in large groups, hemispheric, depressed in the lower part, (90)105–190 µm in diam. Cells of peridium obscure, irregularly shaped, 8-20 µm in diam. Appendages in the basal part of ascocarp, mycelioid, hyaline or yellowish, but not brownish, mainly numerous, (0.5)1- 1.5(2) times as long as the cleistothecial diam., usually simple, rarely irregularly branched, septate. Asci numerous, 5-18, oblong obovoid, stipitate, somewhat unequal-sided, thin- walled, immature in current vegetation period.

Discussion

A preliminary investigation by one of the present authors (Heluta 1999) showed that N. cumminsiana had a more extensive distribution range than it was previously supposed. In addition to America, south eastern Asia, and southern Africa, N. cumminsiana was col- lected in the south of Ukraine (central Europe). This collection was made in 1959, long before its description based on the American specimen. Additional finds of N. cummin- siana in Israel (Fig. 2) and in the Ukraine on new host plants promoted the conclusion that this species could be also found in other regions of western Eurasia, mainly in such tem- perate zones as the Mediterranean region. For example, such powdery mildew fungi as Erysiphe cichoracearum or Oidium erysiphoides s.l. are recorded on different species of genera Crepis and Rhagadiolus from Portugal (Mendonça, Sequeira 1962; Sequeira, Mendonça 1965; Sequeira 1969, 1975, 1978, 1981), Spain (Durrieu, Mercé 1972), Romania (Sandu-Ville 1967; Bontea 1986), and central Europe (Blumer 1967). Some of them may have been easily misidentified, and thus they probably belong to N. cummin- siana. This applies especially to such specimens on which immature ascocarps were men- tioned. “Erysiphe cichoracearum” on L. from Portugal (Sequeira, 1981) may well exemplify the case. According to Amano (1986), Erysiphe cichoracearum was recorded on Phagnalon rupestre and Ph. saxatilis (L.) Cass. in France, on the Balearic and , and in the Spanish Sahara. These specimens very likely belong to N. cum- minsiana. Judging from our analysis of the literature on powdery mildew fungi of Israel, there is rather high probability that collected specimens identified as E. cichoracearum belong to N. cumminsiana. Thus, Rayss (1940, 1947) noted E. cichoracearum, with mainly imma- ture asci, on Crepis aspera L. and C. palaestina (Boiss.) Bornm. Dimensions of its coni- dia and ascocarps corresponded closely with those of N. cumminsiana. In addition, one of these specimens (on Crepis aspera) was collected in Pardes Hanna (Fig. 2), where we found N. cumminsiana on Crepis spp. Also, probability is not excluded that this fungus parasitizes other representatives of the family Asteraceae in Israel. 272 Voityuk & al.: Neoerysiphe cumminsiana (Erysiphales, Eumycota)...

Neoerysiphe cumminsiana has a fairly specific distribution, which does not correspond with the set of probable geographic and mycoflorogenetic units of powdery mildew fungi proposed by Heluta (1993, 1995). It is the only representative of Erysiphales, which must be classified as an American-African-Eurasian South Holarctic species. This supposition is not in accordance with Heluta’s (1992) hypothesis on migration ways of powdery mildew fungi. Thus, we have to assume that this hypothesis is not fully correct, or N. cumminsiana is a complex of morphologically identical species. In the latter case it descended from an ancestor such as N. galeopsidis and probably emerged independently in several regions of America, Africa, or Eurasia. We believe the second supposition is more probable. From this investigation we conclude that N. cumminsiana has a comparatively wide dis- tribution. It seems very likely that it was collected not only in America, eastern Asia, and southern Africa, but also in Israel, plus in countries of southern and central Europe, and northern Africa. However, N. cumminsiana was identified incorrectly as Erysiphe cichoracearum. Hence, an additional revision of powdery mildew specimens collected in these regions on Asteraceae and identified as Erysiphe cichoracearum is necessary, especially those with immature asci. The problem of origin of this fungus has to be clarified, preferably by molecular methods of investigation.

Acknowledgements We thank Dr. Uwe Braun (Germany) for his valuable comments on the manuscript. We wish to express our gratitude to Prof. Solomon P. Wasser (Institute of Evolution, University of Haifa, Israel) for his help and comments on the manuscript, and to Dr. Tatiana V. Andrianova (N.G. Kholodny Institute of Botany, Kiev, Ukraine) for kindly donating a specimen of N. cumminsiana from Phagnalon rupestre.

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Addresses of the authors: Svitlana O. Voityuk a,c, Vasyl P. Heluta b& Eviatar Nevo c aBiological Faculty of Taras Shevchenko Kiev National University, 64 Volodymyrska St., Kiev, 01033, Ukraine. bM.G. Kholodny Institute of Botany, 2 Tereshchenkivska St., Kiev, Ukraine, 01601 cInstitute of Evolution, University of Haifa, Mt. Carmel, Haifa 31905, Israel.